THE NIN-LIKE PROTEIN (NLP) FAMILY IN COMMON BEAN: GENOME-WIDE IDENTIFICATION, EVOLUTION AND EXPRESSION ANALYSIS

One of the plant-specific transcription factor families that play an important role in responses to nitrogen deficiency is NODULE INCEPTION-like (NIN-like) proteins (NLPs). However, the properties and evolutionary relationships of NIN genes in P. vulgaris, which enable nodule formation naturally, have not been studied yet. 12 Pvul-NIN genes have been identified in this study and the approximate positions of these genes have been determined. At the same time, several biochemical and physicochemical properties of NIN-like proteins have been elucidated. Comparisons between both monocot and dicot, but also nodule binding and non-nodule binding species were considered when investigating the evolutionary relationships of NIN genes. 16 duplication events (14 segmental and 2 tandem) have been shown to play a role in the expansion of the NIN gene family in P. vulgaris. In addition, comparative expression analysis of NIN genes was performed by processing publicly available RNAseq data and different levels of Pvul-NIN gene expression under both salt and drought stress were detected, suggesting the roles of Pvul-NIN gene for abiotic stress response. Expression levels of NIN genes have also been investigated in different plant tissues and have been shown to be intensely expressed in nodules and root tissues. This is the first study on the in-silico detection and characterization of Pvul-NIN genes to examine gene expression levels in common bean. The results could therefore provide the basis for future studies of functional characterization of Pvul-NIN genes.

[1]  Hong Liu,et al.  Genome-Wide Identification, Characterization, and Regulation of RWP-RK Gene Family in the Nitrogen-Fixing Clade , 2020, Plants.

[2]  F. Dotta,et al.  Targeting microRNAs as a Therapeutic Strategy to Reduce Oxidative Stress in Diabetes , 2019, International journal of molecular sciences.

[3]  R. Gutiérrez,et al.  Nitrate Induction of Primary Root Growth Requires Cytokinin Signaling in Arabidopsis thaliana. , 2019, Plant & cell physiology.

[4]  Jie Luo,et al.  Growth performance, photosynthesis, and root characteristics are associated with nitrogen use efficiency in six poplar species , 2019, Environmental and Experimental Botany.

[5]  Jie Luo,et al.  Evolutionary analyses of NIN-like proteins in plants and their roles in nitrate signaling , 2019, Cellular and Molecular Life Sciences.

[6]  C. Masclaux-Daubresse,et al.  Morphological and physiological responses to contrasting nitrogen regimes in Populus cathayana is linked to resources allocation and carbon/nitrogen partition , 2019, Environmental and Experimental Botany.

[7]  M. Zhang,et al.  An Essential Role for miRNA167 in Maternal Control of Embryonic and Seed Development1[OPEN] , 2019, Plant Physiology.

[8]  C. Grof,et al.  Profiling the Abiotic Stress Responsive microRNA Landscape of Arabidopsis thaliana , 2019, Plants.

[9]  Trevor M. Nolan,et al.  AP2/ERF Transcription Factor Regulatory Networks in Hormone and Abiotic Stress Responses in Arabidopsis , 2019, Front. Plant Sci..

[10]  C. Masclaux-Daubresse,et al.  Overexpression of ATG8 in Arabidopsis Stimulates Autophagic Activity and Increases Nitrogen Remobilization Efficiency and Grain Filling , 2018, Plant & cell physiology.

[11]  Kun Lu,et al.  Genome-Wide Identification and Characterization of NODULE-INCEPTION-Like Protein (NLP) Family Genes in Brassica napus , 2018, International journal of molecular sciences.

[12]  Y. Tsay,et al.  Nitrate Transport, Signaling, and Use Efficiency. , 2018, Annual review of plant biology.

[13]  A. Good Toward nitrogen-fixing plants , 2018, Science.

[14]  T. Ashman,et al.  The direct effects of plant polyploidy on the legume–rhizobia mutualism , 2018, Annals of botany.

[15]  N. Crawford,et al.  The Arabidopsis NLP7 gene regulates nitrate signaling via NRT1.1–dependent pathway in the presence of ammonium , 2018, Scientific Reports.

[16]  G. Mi,et al.  A RNA-Seq Analysis of the Response of Photosynthetic System to Low Nitrogen Supply in Maize Leaf , 2017, International journal of molecular sciences.

[17]  R. Gutiérrez,et al.  Emerging Players in the Nitrate Signaling Pathway. , 2017, Molecular plant.

[18]  R. Gutiérrez,et al.  Nitrate signaling and early responses in Arabidopsis roots. , 2017, Journal of experimental botany.

[19]  L. Altschmied,et al.  RWP-RK domain-containing transcription factors control cell differentiation during female gametophyte development in Arabidopsis. , 2017, The New phytologist.

[20]  G. Mi,et al.  Within-Leaf Nitrogen Allocation in Adaptation to Low Nitrogen Supply in Maize during Grain-Filling Stage , 2016, Front. Plant Sci..

[21]  J. Stougaard,et al.  micro RNA 172 (miR172) signals epidermal infection and is expressed in cells primed for bacterial invasion in Lotus japonicus roots and nodules. , 2015, The New phytologist.

[22]  G. Mi,et al.  Genetic improvement of root growth increases maize yield via enhanced post-silking nitrogen uptake , 2015 .

[23]  T. Girin,et al.  The plant RWP-RK transcription factors: key regulators of nitrogen responses and of gametophyte development. , 2014, Journal of experimental botany.

[24]  G. Maróti,et al.  Nitrogen-fixing Rhizobium-legume symbiosis: are polyploidy and host peptide-governed symbiont differentiation general principles of endosymbiosis? , 2014, Front. Microbiol..

[25]  S. Polasky,et al.  A tradeoff frontier for global nitrogen use and cereal production , 2014 .

[26]  Mahmut Can Hiz,et al.  Transcriptome Analysis of Salt Tolerant Common Bean (Phaseolus vulgaris L.) under Saline Conditions , 2014, PloS one.

[27]  E. Baudin,et al.  Frequency and intensity of pain related to thyroid nodule fine-needle aspiration cytology. , 2013, Thyroid : official journal of the American Thyroid Association.

[28]  Leon V. Kochian,et al.  Using membrane transporters to improve crops for sustainable food production , 2013, Nature.

[29]  M. Zavolan,et al.  Analysis of CDS-located miRNA target sites suggests that they can effectively inhibit translation , 2013, Genome research.

[30]  Mineko Konishi,et al.  Arabidopsis NIN-like transcription factors have a central role in nitrate signalling , 2013, Nature Communications.

[31]  G. Oldroyd Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants , 2013, Nature Reviews Microbiology.

[32]  Javier F. Palatnik,et al.  Functional Specialization of the Plant miR396 Regulatory Network through Distinct MicroRNA–Target Interactions , 2012, PLoS genetics.

[33]  P. Wittkopp,et al.  Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence , 2011, Nature Reviews Genetics.

[34]  David M. Goodstein,et al.  Phytozome: a comparative platform for green plant genomics , 2011, Nucleic Acids Res..

[35]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[36]  Peer Bork,et al.  Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy , 2011, Nucleic Acids Res..

[37]  F. Daniel-Vedele,et al.  REVIEW: PART OF A SPECIAL ISSUE ON PLANT NUTRITION Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture , 2010 .

[38]  M. Albareda,et al.  Soybean inoculation: Dose, N fertilizer supplementation and rhizobia persistence in soil , 2009 .

[39]  M. Schiavon,et al.  Effects of an alfalfa protein hydrolysate on the gene expression and activity of enzymes of the tricarboxylic acid (TCA) cycle and nitrogen metabolism in Zea mays L. , 2008, Journal of agricultural and food chemistry.

[40]  Emilio Fernández,et al.  Nitrate Signaling by the Regulatory Gene NIT2 in Chlamydomonas[W] , 2007, The Plant Cell Online.

[41]  An-Yuan Guo,et al.  [GSDS: a gene structure display server]. , 2007, Yi chuan = Hereditas.

[42]  Wilfred W. Li,et al.  MEME: discovering and analyzing DNA and protein sequence motifs , 2006, Nucleic Acids Res..

[43]  Peer Bork,et al.  PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments , 2006, Nucleic Acids Res..

[44]  F. Galibert,et al.  Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[45]  J. Vivanco,et al.  Soil nematodes mediate positive interactions between legume plants and rhizobium bacteria , 2005, Planta.

[46]  Yuanji Zhang,et al.  miRU: an automated plant miRNA target prediction server , 2005, Nucleic Acids Res..

[47]  L. Schauser,et al.  Evolution of NIN-Like Proteins in Arabidopsis, Rice, and Lotus japonicus , 2005, Journal of Molecular Evolution.

[48]  M. Hungria,et al.  Benefits of inoculation of the common bean (Phaseolus vulgaris) crop with efficient and competitive Rhizobium tropici strains , 2003, Biology and Fertility of Soils.

[49]  S. Mangan,et al.  Structure and function of the feed-forward loop network motif , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Manuel C. Peitsch,et al.  SWISS-MODEL: an automated protein homology-modeling server , 2003, Nucleic Acids Res..

[51]  Michael Lynch,et al.  Gene Duplication and Evolution , 2002, Science.

[52]  A. Sharrocks The ETS-domain transcription factor family , 2001, Nature Reviews Molecular Cell Biology.

[53]  Leif Schauser,et al.  A plant regulator controlling development of symbiotic root nodules , 1999, Nature.

[54]  C. Schwechheimer,et al.  PLANT TRANSCRIPTION FACTOR STUDIES. , 1998, Annual review of plant physiology and plant molecular biology.

[55]  K. Shinozaki,et al.  Role of arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. , 1997, The Plant cell.

[56]  F. Arnold,et al.  Engineered metal-binding proteins: purification to protein folding. , 1991, Science.

[57]  T. George,et al.  Influence of elevation and applied nitrogen on rhizosphere colonization and competition for nodule occupancy by different rhizobial strains on field-grown soybean and common bean , 1990 .

[58]  P. Gresshoff,et al.  Isolation and properties of soybean [Glycine max (L.) Merr.] mutants that nodulate in the presence of high nitrate concentrations. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[59]  J. Streeter Effect of nitrate in the rooting medium on carbohydrate composition of soybean nodules. , 1981, Plant physiology.

[60]  C. Masclaux-Daubresse,et al.  Source and sink mechanisms of nitrogen transport and use. , 2018, The New phytologist.

[61]  E. Wang,et al.  Effects of intercropping and Rhizobial inoculation on the ammonia-oxidizing microorganisms in rhizospheres of maize and faba bean plants , 2015 .

[62]  M. Sternberg,et al.  Protein structure prediction on the Web: a case study using the Phyre server , 2009, Nature Protocols.

[63]  T. Schwede,et al.  Protein structure homology modeling using SWISS-MODEL workspace , 2008, Nature Protocols.

[64]  R. Voorrips MapChart: software for the graphical presentation of linkage maps and QTLs. , 2002, The Journal of heredity.

[65]  T. N. Bhat,et al.  The Protein Data Bank , 2000, Nucleic Acids Res..

[66]  Z. Yang,et al.  Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. , 2000, Molecular biology and evolution.

[67]  R. Daniel,et al.  Rhizobial denitrification: A review , 1985 .